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Relative ileal amino acid flows and microbial counts in intestinal effluents of Goettingen Minipigs and Saddleback pigs are not different¹

U. Hennig, C. C. Metges, A. Berk, A. Tuchscherer^* and M. Kwella^2,3

¹ Oskar Kellner Research Unit for Nutritional Physiology and and ^* Research Unit Genetics and Biometry, FBN—Research Institute for the Biology of Farm Animals, D 18196 Dummerstorf, Germany and and FAL—Federal Agricultural Research Center, Institute of Animal Nutrition, D 38116 Braunschweig, Germany

	Abstract

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We explored the suitability of Goettingen Minipigs as models to measure ileal AA digestibility and evaluate dietary proteins for conventional pigs. Further, a potential for secondary ileal microbial colonization 5 mo after establishing end-to-end ileorectal anastomosis was investigated. Goettingen Minipigs (BW 18 kg) and Saddleback pigs (BW 27 kg) fitted with end-to-end ileorectal anastomosis were fed six diets based on barley and oilseed meals and three diets based on wheat and milk powder differing in total and ileal digestible lysine. Apparent ileal digestibilities of CP (N x 6.25) and of 20 AA were determined. No differences (P = 0.062 to 0.982) were found in AA apparent ileal digestibilities between breeds. Therefore, Minipigs are a reasonable model to estimate apparent ileal digestibility of AA for evaluation of dietary proteins. However, the apparent ileal digestibility of CP (P = 0.048) was higher in Minipigs than in Saddleback pigs (barley and oilseed meals-based diets 70% vs. 66%; wheat and milk powder-based diets 80% vs. 77%), which is probably due to a smaller contribution of non-AA-nitrogen in the ileal effluent of Goettingen Minipigs. For lysine, the apparent ileal digestibilities (means of both breeds) ranged from 78 to 85% in wheat and milk powder-based, and 70 to 78% in barley and oilseed-based diets. Experimentally derived concentrations of ileally digestible lysine confirmed the values predicted from a published table. Microbial counts were not affected by breed as shown for lactobacilli, with 9.1 ± 0.2 and 9.1 ± 0.2 (P = 0.977), enterococci with 4.8 ± 0.3 and 5.6 ± 0.4 (P = 0.162), and yeasts with 4.6 ± 0.3 and 4.6 ± 0.4 (P = 0.906) log cfu/g effluent for Goettingen Minipigs and Saddleback pigs, respectively. The counts did not change over 5 mo, suggesting that no secondary microbial colonization occurred in pigs with end-to-end ileorectal anastomosis.

	Introduction

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Assessing the ileal digestibility of dietary CP and AA is essential for the evaluation of dietary proteins to calculate feed blends in order to improve the accuracy of diet formulation for pigs, and to reduce environmental nitrogen pollution (Moughan and Smith, 1985; Williams, 1995; Darragh and Hodgkinson, 2000). Compared with conventional pigs, Minipigs are easier to handle and less expensive when tracer-based experiments are being performed owing to their lower body mass (Fassmann, 2001; Backes et al., 2002). Minipigs have been used to study the effects of trypsin inhibitors on protein digestibility (Barth et al., 1993) and to compare the protein flow of endogenous and microbial origin (Bartelt et al., 1994; Bartelt et al., 1999). To the best of our knowledge, Minipigs have not been reported as models for conventional pigs to estimate ileal digestibility of AA for feed evaluation. The measurement of ileal digestibility of AA requires the collection of ileal effluents, which has been done by different cannulation techniques and ileorectal anastomosis (IRA) (Mosenthin and Sauer, 1992; GfE, 2002). We have worked with IRA-pigs because their effluent can be collected quantitatively and no marker is necessary. However, little information is available concerning the microbial composition and counts in ileal effluents of pigs after establishment of ileostoma and IRA (Rowan et al., 1992; Kwella and Hennig, 1996, 1997a) and as affected by different diets (Kwella and Hennig, 1997b).

Thus, the two main objectives of this experiment were to compare both the apparent ileal digestibility (AID) of selected essential AA and the microbial counts in ileal effluents of Goettingen Minipigs (GM) and Saddleback pigs (SP) fitted with IRA, and fed diets differing in ileal digestible lysine and crude protein. A third objective was to quantify the AID of lysine and to explore how this compares with predicted values from a published table (Hennig et al., 1990b).

	Materials and Methods

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Animals and Housing

The experiment was performed with three GM barrows (Ellegard, Dalmose, Denmark) and three SP barrows bred in our own animal facility (FBN, Dummerstorf, Germany). The experimental protocol was approved by the ethics committee of the Ministry of Nutrition, Agriculture, Forestry, and Fishery, Schwerin, State Mecklenburg-Vorpommern, Germany (Permission No. 7221/3-013/93). Three weeks before starting the investigations, the animals were fitted with an end-to-end IRA (EEV-IRA) conserving the ileocecal valve and to isolate the colon completely, according to Hennig et al. (1990a) and Laplace et al. (1994). The postsurgical care during 14 d of convalescence included daily wound treatments, rinsing of the colon cannula, cleaning of the anal area and daily drinks of chamomile tea to aid the wound healing. After surgery, food supply was increased slowly and full presurgical food intake was resumed on d 11. The pigs were housed individually in floor pens and during collection periods in metabolic cages. The animals were washed daily with warm water and soap.

Diets and Feeding

Three different diet types were designed using common dietary components for fattening pigs (Table 1). Diet 1 and 3 consisted of barley, rye, and oilseed by-products, whereas Diet 2 contained wheat, triticale, and skim milk powder. The main ingredients of Diet 1 and 3 were of lower digestibility than the ingredients of Diet 2. Diets were formulated based on lysine and methionine AID using total Lys and Met content of all ingredients and published digestibility coefficients of Hennig et al. (1990b). Thus, the level of apparent ileally digestible lysine was lower in Diet 1 than in Diet 2 despite an equal total Lys content. Diet 3 was equivalent to Diet 1 in the main ingredients but supplemented with L-lysine•HCl and DL-methionine to obtain equivalent levels of AID lysine and methionine as in Diet 2 (Table 1). The analyzed total lysine content in Diet 1 was somewhat higher than intended but the difference in AID lysine was maintained (Table 1). Crystalline glycine and L-leucine were added to adjust the level of amino nitrogen.

Every trial period consisted of 7 d (Table 2), that is, 4 d for adaptation and 3 d for collection of ileal effluents without using a marker (Mariscal-Landin et al., 1995; GfE, 2002). Effluents were quantitatively collected in a mixture of ethanol and formaldehyde (99.5:0.5; vol/vol) to abolish microbial activity and stored at 4°C. At the end of each collection period, total effluent was weighed and homogenized, and samples were taken for analysis. The sample weights were recorded before and after lyophilization. Dried effluents were ground to pass a 1-mm sieve using an AM-1 grinder (F. K. Retsch GmbH and Co. KG, Haan, Germany), and the DM content was determined (10 h at 60°C).

Nitrogen content was analyzed using a standard Kjeldahl procedure (AOAC, 1995). Three hydrolysates of two samples of each diet and dried effluents of all individual animals were prepared. Cystine and methionine were determined as cysteic acid and methionine sulfone after oxidation with performic acid (16 h at 0°C) followed by hydrolysis with 6 N HCl (22 h at 110°C). An alkaline hydrolysis was used to determine tryptophan (4 N NaOH, 26 h at 110°C). All other AA were determined following 6 N HCl hydrolysis (22 h at 110°C). No corrections were made for losses of AA during hydrolysis. The AA contents in the dried effluents and diets were determined quantitatively with liquid ion exchange chromatography (Biochrom 20; Pharmacia LKB Biochrom Ltd., Cambridge, U.K.).

Samples for microbiological investigations were taken 1 d before the quantitative collection of the ileal effluent. After the morning cleaning of the metabolic cages, the next effluent discharged by each pig was sampled as soon as possible; 10 g of each sample was suspended in 90 mL of 0.85% (wt/vol) sodium chloride solution and homogenized, followed by 10-fold serial dilutions. The dehydrated culture media (SIFIN, Berlin, Germany) and culture conditions used to determine counts (log₁₀ of colony-forming units) of the microbial groups are summarized in Table 4.

The daily ileal flows of AA and CP were calculated from digesta DM (kg/d) x digesta DM AA concentration (g/kg). The AID of individual AA and CP were computed according to the following equation:

where AA intake is DMI (kg/d) x AA content in DM (g/kg). Ileal flow and AID was also calculated for the sum of all 20 AA determined.

The dietary content of AID lysine (g/kg) was calculated by multiplication of analyzed dietary total lysine with the experimentally derived AID of lysine in all animals and treatments. The experimentally derived dietary lysine content was compared with predicted values based on published AID (Hennig et al., 1990b).

Statistical analysis was done with SAS using the procedure MIXED of SAS/STAT software, Version 8.2 (SAS Inst. Inc., Cary, NC). The general linear model

was used, where y denotes the vector of observations, X the known design matrix, ß the unknown vector of fixed effects (breed, diet, diet subtype, and all interactions), and is the vector of random errors, with expectation 0 and covariance matrix R. Repeated measures of the animals were taken into account by the repeated statement of PROC MIXED to specify the R matrix in the model. The minimum variance quadratic unbiased estimation () of the covariance parameters was used.

The significance of each of the main effects and interactions in the model were tested by the linear hypothesis H₀:Lß = 0 (Type 3 tests of fixed effects) using the following F-statistic: F = {'L'[L(X'^–1X)^—L']^—L}/rank(L), with = (X'^–1X)^—X'^–1y.

The MIXED procedure checks whether a fixed effect changes within any subject. If so, it assigns within-subject degrees of freedom to the effect; otherwise, it assigns the between-subject degrees of freedom to the effect (Schluchter and Elashoff 1990). If there are multiple within-subject effects containing classification variables, the within-subject df are partitioned into components corresponding to the subject x effect interactions. Differences at P-values <0.05 were considered to be significant.

Least squares means (LSM) of variables and differences between LSM were computed. Each LSM was computed as L, where L is the coefficient matrix associated with the LSM and is the estimate of the fixed-effects parameter vector. The approximate standard errors for the LSM is computed as the square root of L(X'^–1X)^–L'.

	Results

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Dietary Intakes, Flows, and Digestibilities of Crude Protein and Amino Acids

The content of CP in Diets 1 and 3 were comparable and somewhat lower than in Diet 2 (Table 1). Target amounts of total lysine in Diets 1 and 2 should be similar but lower than in Diet 3. Owing to the variation of protein and/or lysine content in feed components, the total lysine concentrations in two subtypes of Diet 1 were slightly higher than in the corresponding subtypes of Diet 2. All subtypes of Diet 3 were higher in total lysine than in Diet 1 as a result of the L-lysine supplementation. The energy content (ME, megajoules per kilogram), calculated by means of analyzed crude nutrients was similar in all diets (Table 1).

The mean daily DMI in GM was lower than in SP over the total experimental period due to the lower BW of GM (Table 3) and corresponded to 71 (61 to 79) and 78 (75 to 82) g•kg BW^0.75•d^–1 in GM and SP, respectively.

The flows of CP, all individual AA and the sum of all AA in ileal effluents of GM were significantly lower than those of SP (Table 5) owing to the lower DMI in GM. However, irrespective of the lower DMI, the flow patterns of AA (g/16 g N) in ileal effluents were not different between GM and SP (data not shown). Expressed per kilogram BW, total ileal flows for lysine, threonine, methionine, cystine, and tryptophan were 41 to 61, 42 to 61, 14 to 24, 19 to 27, and 9 to 15 mg•kg^–1•d^–1, respectively, where the lower values were due to the milk protein-based Diet 2.

The daily flows of CP, Thr, Met, Cys, Trp, and the sum of all AA were affected by diet (P = 0.001 to 0.012) as shown in Table 5. In general, flows with Diet 2 are lower than with Diet 1 or 3. No significant interactions of breed x diet, diet x subtype, and diet x subtype x breed were found for the flows of CP and all AA. Only the interaction subtype x breed shows significant differences for CP (P = 0.011) and tryptophan (P = 0.032).

There was no breed effect on AID for each of the five most-limiting AA and all other AA measured (data not shown) or of the sum of all AA (Table 6). The CP values were different for GM and SP (P = 0.048), especially when Diet 1-M was fed (71 vs. 62%).

The mean estimated dietary content of AID lysine (grams per kilogram DM) using the experimentally derived AID of lysine of all animals of both breeds is shown in Figure 1. These results are in reasonable agreement with previously calculated AID lysine content based on the total lysine content of each component multiplied by digestibility coefficients (Hennig et al., 1990b).

View larger version (26K): [in this window] [in a new window]   Figure 1. Calculated apparent ileal digestible lysine content (circles, ) based on total lysine for each component multiplied by digestibility coefficients (Hennig et al., 1990b) and measured concentrations of apparent ileal digestible lysine (grams per kilogram DM) in three different diets. Bars are least squares means ± SE of Goettingen Minipigs (empty bars) and Saddleback pigs (shaded bars); three animals and two repetitions for each bar. Diet 1 and 3 were based on barley and oilseed meals; Diet 2 was based on wheat and milk powder. The letters E, M, and F stand for three subtypes of the three diets with different CP concentrations designed for early, middle, and finishing growing stages (see Table 1).

Microbial counts of lactobacilli, enterococci, and yeast, expressed as LSM of log colony-forming units per gram effluent, are detailed shown in Table 7. They were in the range of 9 for lactobacilli and in the range of 4 for yeasts in both breeds. The numbers of enterococci were numerically lower in GM than in SP (4.8 vs. 5.6). Microbial counts were not affected by breed as shown for lactobacilli with 9.1 ± 0.2 and 9.1 ± 0.2 (P = 0.977), enterococci with 4.8 ± 0.3 and 5.6 ± 0.4 (P = 0.162), and yeasts with 4.6 ± 0.3 and 4.6 ± 0.4 (P = 0.906) log cfu/g effluent for GM and SP, respectively. Over the total experimental period of approximately 5 mo, no changes in microbial counts occurred both in GM and SP. In addition, diets did not affect microbial counts.

	Discussion

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Flows and Digestibilities of Crude Protein and Amino Acids

Large differences in the small intestinal tract length and weight between miniature and conventional pigs occur as described by Holtz and Kallweit (1981) and Kühn (2001). As a consequence, these two groups of animals show a different DMI and flows of CP and AA. In spite of these differences, the DMI related to body weight (g•kg BW^0.75) was not different between breeds, and, consequently, there were no differences in AID of all individual indispensable and dispensable AA as presented for the five most-limiting AA for growing pigs (remaining AA not shown; Table 6). The AID of CP, however, was lower in SP than in GM (P = 0.048). Different feed intakes between breeds are not likely to affect the ileal AA digestibility coefficients, as observed previously (Haydon et al., 1984; Albin et al., 2001). Only extremely different feed intakes in restrictively fed growers as compared with ad libitum fed sows led to differences in AID of AA (Stein et al., 1999). We believe that the lower AID of CP in SP might be due to a difference in the distribution of AA-nitrogen and non-AA-nitrogen and the contribution of endogenous nitrogen in the ileal effluents. Because protein digestibilities were calculated based on Kjeldahl-N x 6.25, we also compared the CP flows with the sum of all AA flow in ileal effluents (Table 5). The total ileal flows of the sum of all AA expressed as a percentage of CP flows were lower in SP than in GM with the exception of Diet 1-E and Diet 3-E. Over all diets, there was a smaller contribution of all AA in relation to CP in SP as compared with GM, which indicates a higher level of non-AA-nitrogen in effluents of SP (33 vs. 29%). In Minipigs, a lower total endogenous nitrogen fraction passing the ileum compared with Landrace pigs has been found by Bartelt et al. (1999). With reference to our results, we assume that a lower level of non-AA-nitrogen (e.g., urea; Mosenthin et al., 1994) in the ileal effluent of GM might explain the higher CP digestibility, which is without any implications for the AID of AA.

The AA in ileal effluents are of dietary and endogenous origin. Based on endogenous flows earlier determined in our laboratory (Wünsche et al., 1979), calculation of endogenous ileal lysine and threonine flows in our pigs of both breeds resulted in values of 14 and 19 mg•kg^–1•d^–1, respectively. In the present experiment, total ileal lysine and threonine flows were between 40 mg•kg^–1•d^–1 in the wheat and milk powder–based diet (Diet 2) and 60 mg•kg^–1•d^–1 in barley and oilseed–based diets (Diet 1, Diet 3). This can be explained by higher losses owing to feed-specific endogenous flows and undigested losses with experimental Diets 1 and 3 compared with the milk powder-based Diet 2 (Diet 2: lysine 26 and threonine 21 mg•kg^–1•d^–1 and Diets 1 and 3: lysine 46 and threonine 41 mg•kg^–1•d^–1) and further indicates that diets containing animal protein result in lower ileal AA losses.

The AID of AA at the end of ileum is a result of the small intestinal digestion of protein, absorption of the dietary AA, and secretion and reabsorption of endogenous AA. In the barley- and oilseed meal-based diets, the lowest AID was observed for threonine (Table 6). This is possibly due to both a lower absorption of the dietary threonine and a higher contribution of endogenous threonine in the effluent. Threonine represents the AA with the highest concentration among indispensable AA of endogenous origin in pigs (De Lange et al., 1989). In order to minimize the effect of endogenous threonine losses on the AID, the dietary concentration of threonine in test diets was recommended to be 7 g/kg DM (GfE, 2002). In Diets 1 and 3, threonine concentrations were not high enough to eliminate entirely the effect of endogenous threonine losses on the digestibility coefficients. In spite of a sometimes lower total dietary threonine concentration in Diet 2 (wheat and milk powder) compared with Diets 1 and 3, the absorption of threonine is higher in Diet 2 probably as a result of the animal protein source (Table 6). In IRA pigs fed a similar diet (wheat, casein, and fish meal) comparable ileal AA flows were found as in our experimental Diet 2 and the AID was lowest for threonine and highest for methionine (Laplace et al., 1994), which corresponds with our results. In the barley- and oilseed-based diets (Diets 1 and 3) we found the highest AID for sulfur AA, again followed by lysine, tryptophan, and threonine.

It has been proposed earlier to apply the AID of individual AA to improve the accuracy of diet formulation (Williams, 1995). Here we confirm that predicted AID values of dietary components (Hennig et al., 1990b) agree with experimentally derived AID values in both breeds (Figure 1). The validity of the proposal by Williams (1995) has been also demonstrated in a pig fattening experiment by Schulz et al. (1999). These authors used identical diets as in the present experiment. Their results demonstrated that pigs fed Diet 1 showed impaired growth and N-balances compared with Diets 2 and 3 owing to the lower intake of ileal digestible lysine. After intake of Diet 3, the daily BW gain and energy expenditure were equivalent compared with pigs fed Diet 2, whereas pigs fed Diet 1 showed significantly increased energy expenditure but a decreased daily BW gain.

Microbiological Investigations

Most investigations of intestinal microflora were done in piglets and in particular weaners. If there are results from older pigs, the microbes were frequently counted in fecal samples only or the study was only concerned with enterobacteria.

The microbial counts in the effluent of our pigs with EEV-IRA are in the same range as reported for ileal digesta of intact pigs (Pesti, 1962; Smith, 1965). Similar counts of small intestinal bacteria are also reported by Schulze and Bathke (1977) and Jensen (1998) for ileal digesta of slaughtered pigs. To compare microbiological counts between various reports is difficult because of the diversity in fed diets, additives, and various microbiological media and techniques (van der Heyde, 1973).

The microbial counts of lactobacilli, enterococci, and yeasts after establishing the ileorectal anastomosis were not altered during the experimental period of 5 mo. This finding suggests that no secondary microbial colonization in the terminal ileum of EEV-IRA pigs occurred, in contrast to ileostomy as described in humans and pigs (Vince et al., 1973; Rowan et al., 1992) and to IRA with an open colon (Köhler et al., 1992). Ileostomy is obviously quite different from the surgical technique we applied (i.e., an EEV-IRA including the intact ileocecal valve and complete isolation of the large intestine). It has been demonstrated that the conservation of the ileocecal valve is crucial to sustain normal physiological functions of the small intestine (Gazet and Kopp, 1964).

We conclude from our results that the EEV-IRA technique used here is suitable to study the ileal flows of AA in long-term investigations, which confirms previous histological results (Redlich et al., 1997).

	Implications

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In view of the comparable amino acid flow patterns and equal apparent ileal digestibility in both breeds investigated, Goettingen Minipigs are suggested to be a suitable model to assess the ileal digestibility of amino acids for feed evaluation. However, the higher apparent ileal digestibility of crude protein in Goettingen Minipigs compared with Saddleback pigs suggests that caution is indicated in the use of Saddleback pigs for CP digestibility. The fact that the counts of lactobacilli, enterococci, and yeasts in ileal effluents of both breeds after ileorectostomy are in the range as previously reported elsewhere after slaughtering, and that there were no time- or diet-dependent alterations, illustrates that our surgical procedure applied is not accompanied by alterations of intestinal microbial flora.

	Footnotes

 
¹ The study was funded by the core budget to the Res. Inst. for the Biology of Farm Animals.

³ The authors acknowledge R. Gaeth and W. Booth for animal care, sampling of ileal effluents, and microbiological examinations. We are grateful to W. B. Souffrant, Ch. Voight, U. Lüdtke, and M. Gratopp for analyses of N and AA. We also thank the associate editor and the reviewers for their helpful comments.

² Correspondence—phone: 0493820868672; fax: 0493820868652; e-mail: kwella{at}fbn-dummerstorf.de.

Received for publication October 10, 2002. Accepted for publication February 12, 2004.

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